United States Environmental

Protection Agency

Office of Water

Washington, DC 20460

EPA-822-R-02-024

March 2002

Methods for evaluating wetland condition

#16 Vegetation-Based Indicators of

Wetland Nutrient Enrichment
United States Environmental

Protection Agency

Office of Water

Washington, DC 20460

EPA-822-R-02-024

March 2002

Methods for evaluating wetland condition

#16 Vegetation-Based Indicators of

Wetland Nutrient Enrichment

Principal Contributor

Indiana University, School of Public and Environmental Affairs

Christopher Craft

Prepared jointly by:

The U.S. Environmental Protection Agency

Health and Ecological Criteria Division (Office of Science and Technology)

and

Wetlands Division (Office of Wetlands, Oceans, and Watersheds)
United States Environmental

Protection Agency

Office of Water

Washington, DC 20460

EPA-822-R-02-024

March 2002

Notice

The material in this document has been subjected to U.S. Environmental Protection Agency (EPA)

technical review and has been approved for publication as an EPA document. The information

contained herein is offered to the reader as a review of the “state of the science” concerning wetland

bioassessment and nutrient enrichment and is not intended to be prescriptive guidance or firm advice.

Mention of trade names, products or services does not convey, and should not be interpreted as

conveying official EPA approval, endorsement, or recommendation.

Appropriate Citation

U.S. EPA. 2002. Methods for Evaluating Wetland Condition: Vegetation-Based Indicators of

Wetland Nutrient Enrichment. Office of Water, U.S. Environmental Protection Agency, Washington, DC. EPA-822-R-02-024.

This entire document can be downloaded from the following U.S. EPA websites:

http://www.epa.gov/ost/standards

http://www.epa.gov/owow/wetlands/bawwg

ii
iii

Contents

Foreword................................................................................................................... v

List of Modules ........................................................................................................ vi

Summary ...................................................................................................................... 1

Purpose....................................................................................................................... 1

Introduction.............................................................................................................. 1

Vegetation-Based Indicators of Nutrient Enrichment ................................. 2

Methods for Assessing Nutrient Enrichment ................................................ 6

Case Studies ............................................................................................................ 11

References ..............................................................................................................19

Glossary .................................................................................................................. 22

List of Tables

Table 1: Level I and Level II Indicators of Nutrient

Enrichment in Wetlands.................................................................12

Table 2: Comparison of Vegetation-Based Indicators of

Phosphorus (P) Enrichment in Unenriched and

Eutrophic Sawgrass, Cladium jamaicense,

Communities of the Florida Everglades ...................................14

Table 3: Level I and Level II Indicators of Phosphorus (P)

Enrichment of Sawgrass, Cladium jamaicense,

Communities of the Florida Everglades ...................................15

Table 4: Level I and Level II Indicators of Nitrogen (N)

Enrichment of Spartina alterniflora Dominated

Salt Marshes Along the Atlantic (NC, GA) Coast .................17
iv

Table 5: Level I and Level II Indicators of Nitrogen (N)

and Phosphorus (P) Enrichment of a Wet Sedge

Tundra (Eriophorum angustifolium) in Alaska After

5 Years of Fertilization................................................................. 18

LIST OF FIGURES

Figure 1: Distribution of Plant Species and Hydroperiod

Across a Southeastern Bottomland Forested

Wetland................................................................................................. 9

Figure 2: Distribution of Plant Species and Hydroperiod

Across a Freshwater Marsh Wetland......................................... 9

Figure 3: Protocol for Sampling Vegetation for Wetland

Eutrophication Assessments ...................................................... 10
v

Foreword

In 1999, the U.S. Environmental Protection Agency (EPA) began work on this series of reports entitled

Methods for Evaluating Wetland Condition. The purpose of these reports is to help States and

Tribes develop methods to evaluate (1) the overall ecological condition of wetlands using biological

assessments and (2) nutrient enrichment of wetlands, which is one of the primary stressors damaging

wetlands in many parts of the country. This information is intended to serve as a starting point for States

and Tribes to eventually establish biological and nutrient water quality criteria specifically refined for

wetland waterbodies.

This purpose was to be accomplished by providing a series of “state of the science” modules concerning

wetland bioassessment as well as the nutrient enrichment of wetlands. The individual module format

was used instead of one large publication to facilitate the addition of other reports as wetland science

progresses and wetlands are further incorporated into water quality programs. Also, this modular

approach allows EPA to revise reports without having to reprint them all. A list of the inaugural set of

20 modules can be found at the end of this section.

This series of reports is the product of a collaborative effort between EPA’s Health and Ecological

Criteria Division of the Office of Science and Technology (OST) and the Wetlands Division of the

Office of Wetlands, Oceans and Watersheds (OWOW). The reports were initiated with the support

and oversight of Thomas J. Danielson (OWOW), Amanda K. Parker and Susan K. Jackson (OST),

and seen to completion by Douglas G. Hoskins (OWOW) and Ifeyinwa F. Davis (OST). EPA relied

heavily on the input, recommendations, and energy of several panels of experts, which unfortunately

have too many members to list individually:

n Biological Assessment of Wetlands Workgroup

n Wetlands Nutrient Criteria Workgroup

More information about biological and nutrient criteria is available at the following EPA website:

http://www.epa.gov/ost/standards

More information about wetland biological assessments is available at the following EPA website:

http://www.epa.gov/owow/wetlands/bawwg
vi

List of “Methods for Evaluating Wetland

Condition” Modules

1 ................. Introduction to Wetland Biological Assessment

2 ................. Introduction to Wetland Nutrient Assessment

3 ................. The State of Wetland Science

4 ................. Study Design for Monitoring Wetlands

5 ................. Administrative Framework for the Implementation of a

Wetland Bioassessment Program

6 ................. Developing Metrics and Indexes of Biological Integrity

7 ................. Wetlands Classification

8 ................. Volunteers and Wetland Biomonitoring

9 ................. Developing an Invertebrate Index of Biological

Integrity for Wetlands

10............... Using Vegetation to Assess Environmental Conditions

in Wetlands

11 ............... Using Algae to Assess Environmental Conditions in

Wetlands

12 ............... Using amphibians in Bioassessments of Wetlands

13 ............... Biological Assessment Methods for Birds

14 ............... Wetland Bioassessment Case Studies

15 ............... Bioassessment Methods for Fish

16 ............... Vegetation-Based Indicators of Wetland Nutrient

Enrichment

17 ............... Land-Use Characterization for Nutrient and Sediment

Risk Assessment

18............... Biogeochemical Indicators

19 ............... Nutrient Load Estimation

20 .............. Sustainable Nutrient Loading

Module # Module Title
1

Summary

V egetation-based attributes of wetland function (e.g., energy flow, nutrient cycling) and

structure (species composition) that respond to

nutrient enrichment and eutrophication are presented below. Attributes consist of Level I and

Level II indicators that respond quickly to nutrient enrichment and are relatively easy to use.

Level I indicators consist of remotely sensed data

to assess change in wetland plant communities

over time as well as field measurements of stem

height and leaf C:N:P ratios. Level I indicators

are recommended for coarse assessment of individual wetlands or large-scale surveys of many

wetlands. Level II indicators include

aboveground biomass/litterfall, standing dead

C:N:P, nutrient resorption efficiency and proficiency, nutrient use efficiency, and nutrient-tolerant and -intolerant species. These indicators

are used for more detailed assessment of wetland eutrophication. Their sound application requires that similar sample collection protocols

be used for both “targeted” (potentially eutrophic)

and reference (unenriched) wetlands.

Observational and experimental studies confirm

the reliability of vegetation-based indicators for

identifying eutrophication in nutrient-enriched

and unenriched areas of the Florida Everglades,

salt marshes, and wet sedge tundra. Until the

indicators are tested elsewhere, however, they

should be applied cautiously to assessments of

eutrophication in other types of wetland and in

different geographic regions.

Purpose

T

he purpose of this module is to identify veg

etation-based indicators that can be used by

wetland regulatory and natural resource managers to determine the nutrient status (eutrophic or

unenriched) of freshwater and estuarine wetlands.

Introduction

W etlands improve surface water quality byintercepting sediment, nutrients, and other

pollutants transported from terrestrial areas and

upstream aquatic ecosystems (Johnston 1991,

Mitsch and Gosselink 1993). Wetlands become

sinks for nitrogen (N) by sequestering it in accumulating soil organic matter (Craft 1997) and by

microbially converting nitrate (NO3

-

) to atmospheric N2

 (denitrification) (Groffman 1994).

Wetlands serve as sinks for phosphorus (P) by

trapping sediments; by sorption to iron (Fe), aluminum (Al), and calcium (Ca) minerals; and by

plant uptake (Craft 1997). The ability of wetlands to remove nutrients has led to its widespread use, in both natural and artificial forms,

to remove N and P from secondarily treated

wastewater, septic effluent, and nutrient-enriched

agricultural drainage (Johnston et al. 1991, Craft

and Richardson 1993, Kadlec and Knight 1996).

When natural wetlands receive excessive nutrient loadings, ecosystem processes, such as plant

productivity and nutrient cycling, are altered in

measurable ways. The structure of the plant community also may change as slower growing native species are replaced by faster growing species that take advantage of high nutrient levels to

increase growth (Davis 1991).

The threshold where significant alteration in

wetland function and structure occurs is referred

to as the “assimilative capacity” of the system.

When the assimilative capacity of a wetland is

exceeded, the ecosystem responds by increasing

nutrient uptake that translates into increased

growth. Sometimes the result is a shift in plant

species composition, as natives are displaced

by aggressive interlopers like cattail (Typha).

This phenomenon is known as cultural eutrophication and is caused by excessive nutrient loadings from anthropogenic sources. Because N and

P are the primary nutrients limiting productivity

in wetlands (Schlesinger 1991, Vitousek and
2

Howarth 1991, Bridgham et al. 1996), these nutrients usually are responsible for changes in ecosystem function and structure that occur when wetland

assimilative capacity is exceeded (Carpenter et al.

1998).

Wetland vegetation responds to nutrient additions by increased storage of N and P in plant

tissue and by increased net primary production

(NPP) (Craft et al. 1995, Bridgham et al. 1996).

Increased NPP and nutrient storage in turn affect

ecosystem processes including decomposition

(Valiela et al. 1982, Davis 1991, Rybczyk et al.

1996), accumulation of soil organic matter, and

organic carbon export (Craft and Richardson

1993, 1998, Morris and Bradley 1999). Over

time, plant species composition may shift as native species decline and are replaced by species

that take advantage of high nutrient levels to increase growth (Craft et al. 1995). Nutrient enrichment often results in replacement of uncommon or rare species by species tolerant of high

nutrient loadings (e.g., Typha, Phragmites)

(Davis 1991, Chambers et al. 1999, Galatowitsch

et al. 1999). Such changes in community

composition and ecosystem processes

compromise wetland ecological integrity by

altering energy flow, nutrient cycling, and

niche/habitat characteristics that in turn affect

wetland fauna assemblages.

This chapter describes vegetation-based indicators that can be used to determine whether a

wetland’s ecological integrity has been impaired

by nutrient enrichment and eutrophication. Indicators are described for structural and functional responses to both low and high nutrient

loadings. Functional indicators include leaf N

and P content and metrics of NPP (biomass production, stem height). Structural indicators consist of the presence/absence of “sentinel” species that reflect ambient (low nutrients) and impaired (high nutrients) nutrient loading regimes.

Methods for sampling vegetation and analytical

techniques to assess the degree of nutrient enrichment also are described.

Vegetation-Based

Indicators of

Nutrient Enrichment

N

utrient enrichment affects both structural and

functional attributes of wetlands. Structural

attributes include characteristics of the community, or of individual species, whereas functional

attributes relate to energy flow and nutrient cycling. Changes in wetland function that occur in

response to nutrient enrichment include increased

N and P uptake, NPP, and decomposition.

Changes in structure occur through shifts in plant

species composition, including replacement of

nutrient-intolerant species with those adapted to

high nutrient conditions. In this module, functional indicators are emphasized because energy

flow and nutrient cycling processes respond

quickly and dramatically when nutrient loadings

are increased.

Functional Indicators

When nutrients are limiting, wetland vegetation responds to nutrient additions by incorporating N and P into growing or “green” tissue

and increasing NPP (Shaver and Melillo 1984,

Craft et al. 1995, Koerselman and Meuleman

1996, Shaver et al. 1998). Changes in nutrient

uptake and NPP affect wetland energy and nutrient cycles by altering rates of uptake, storage,

and release of C, N, and P.

Net primary productivity

Net primary productivity is the amount of carbon fixed during photosynthesis that is incorporated into new leaves, stems, and roots. NPP is

often expressed as amount of biomass produced

per m2 of wetland surface per year (g/m2/yr). Most
3

techniques to measure NPP focus on production of

aboveground biomass and discount root production that sometimes accounts for half or more of the

NPP. The simplest way to measure aboveground

biomass is by harvesting all of the standing material

at the end of the growing season (Broome et al.

1986). This method is useful for measuring NPP of

herbaceous emergent vegetation, especially in temperate climates where there is a distinct growing

season. However, measurements of aboveground

or “standing crop” biomass typically underestimate

NPP because they do not include biomass losses

to herbivory and stem mortality during the growing

season. Nondestructive methods such as tagged

stems or the use of external markers like wire are

used to measure NPP of Sphagnum (Clymo and

Hayward 1982) and coastal Louisiana marsh plants

(Hopkinson et al. 1980). These methods account

for stem mortality and herbivory, and provide a truer

estimate of NPP than the harvest method. However, they are much more labor-intensive, and timeconsuming, and are not recommended for wetland

eutrophication assessment. Enhanced biomass production is reflected by increased height and, sometimes, stem density of herbaceous emergent vegetation (Broome et al 1983). Increased stem density, however, may reflect other factors like vigorous clonal growth, so it is not recommended as an

indicator of nutrient enrichment.

Woody vegetation is not as good an indicator

of enrichment as is herbaceous vegetation.

Woody plants grow slowly and have a longer

life cycle than herbaceous plants, resulting in a

slower response to nutrient loading. In wetland

dominated by trees with little herbaceous vegetation, leaf litterfall is a common means to estimate NPP (Chapman 1986). Measurements of

litterfall involve the periodic (usually monthly)

collection of leaf litter that collects in littertraps

placed on or above the forest floor. Like the

harvest method, litterfall is an index of NPP because it estimates the portion of NPP that goes into

producing photosynthetic tissue. One drawback,

however, is that the litterfall method is labor-intensive and time-consuming. But, for wetlands where

herbaceous vegetation is unimportant, litterfall is the

best method to measure NPP.

Biogeochemical cycling

Indicators of biogeochemical cycling describe

the uptake, storage, and release of N and P in

plant tissue. Nutrient enrichment of wetlands

leads to increased uptake and storage of N and/

or P, depending on the causative nutrient

(Verhoeven and Schmitz 1991, Shaver et al.

1998). In wetlands where P is limiting, leaf tissue P is the first indicator to respond to nutrient

enrichment (Craft et al. 1995). Increased P uptake by plants is known as “luxury uptake” because P is stored in vacuoles and used later

(Davis 1991). Like P, leaf tissue N increases in

response to N enrichment (Brinson et al. 1984,

Shaver et al. 1998). However, most N is used

directly to support photosynthesis and growth of

new tissue, so luxury uptake of N is not always

observed (Verhoeven and Schmitz 1991).

The ratio of carbon to nitrogen (C:N) in

aboveground biomass or leaves can be used to

determine whether a wetland is N-limited or

whether there is excess N in the system. Under

conditions of N enrichment, plants assimilate

more N, increasing leaf N and decreasing C:N

(Shaver and Melillo 1984, Shaver et al. 1998).

Likewise, P enrichment results in increased leaf

P and decreased C:P (Craft et al. 1995). Application of C:N and C:P ratios requires that

baseline measurements are made using vegetation collected from unenriched areas or from the

same area prior to eutrophication.

Leaf N:P also has been used to determine

whether a wetland is N-limited or P-limited

(Koerselman and Meulemen 1996, Verhoeven et

al. 1996). It has been hypothesized that N:P < 15

(weight:weight basis) indicates N limitation whereas
4

N:P>15 indicates P limitation (Verhoeven et al.

1996). Assuming that this hypothesis is valid, this

information is useful for determining whether a wetland is at risk for either N or P enrichment. For

example, wetlands with vegetation N:P<15 may be

susceptible to N enrichment whereas wetlands with

vegetation N:P>15 may be susceptible to P limitation. Sometimes N:P ratios are presented on a

mole:mole basis. In this case, N:P <33 indicates N

limitation whereas N:P>33 suggests P limitation.

Development of techniques to identify N versus P

limitation is important because, for a given wetland,

the nutrient that limits ecosystem productivity usually is the cause of eutrophication.

Three useful measures of nutrient availability

and eutrophication are nutrient resorption efficiency, nutrient resorption proficiency, and nutrient use efficiency (Shaver and Melillo 1984,

Killingbeck 1996). Nutrient resorption efficiency

is a measure of nutrient conservation and limitation. Under low nutrient conditions, plants resorb and translocate nutrients from senescing tissue and store them in belowground tissue to be

used later (Aerts et al. 1999). Vegetation growing in nutrient-poor wetlands translocate large

quantities of nutrients to belowground tissue and,

thus, possess high nutrient resorption efficiency.

Plants growing in nutrient-enriched wetlands often possess low nutrient resorption efficiency

because of high nutrient availability in soil and

water. Nutrient resorption efficiency (RE) is

defined as:

where biomass is aboveground clipped (harvested) material.

Resorption efficiency also may be calculated using the concentration of N or P (mg) per individual

leaf (Aerts et al. 1999) or per cm2 leaf material

(Feller et al. 1999).

Nitrogen and P in senesced or standing dead

leaves also are used as measures of nutrient resorption proficiency. Nutrient resorption proficiency is

defined as the absolute levels to which nutrients are

reduced in senesced leaves (Killingbeck 1996).

Resorption is highly proficient in plants that reduce

N and P concentrations below 0.7% and 0.05%,

respectively. It is thought that high resorption proficiency is an evolutionary adaptation that enables

plants to conserve nutrients in infertile environments

(Killingbeck 1996).

Nutrient use efficiency (NUE) is a measure of

the effectiveness by which plants use nutrients

to produce biomass. High NUE corresponds to

high rates of nutrient resorption because large

amounts of biomass are produced with little loss

of nutrients in litterfall (Vitousek 1982). Nutrient-poor wetlands often possess lower litter N

and P concentrations, resulting in a higher NUE

than in nutrient-rich wetlands (see Table 2).

Nutrient use efficiency is defined as:

where litterfall/biomass and nutrients are

expressed in g/m2 (Vitousek 1982).

A simpler means to measure NUE is by calculating the inverse of the concentration of N or P

in standing dead biomass/litterfall (Aerts et al.

1999). The major advantage of this method over

the standard NUE method is that litterfall need

not be measured, only tissue N and/or P content.

Nutrient use efficiency varies widely among differAboveground biomass production

(e.g., litterfall, standing dead biomass)

Nutrient (N or P) in litterfall,

standing dead biomass

NUE =

N or P (g/m2) in green biomass

minus N or P (g/m2) in standing

dead biomass

N or P (g/m2) in green biomass RE = x 100 %
5

ent growth forms such as grasses, conifers, and

deciduous trees and shrubs. For example, conifers

typically have much higher N and P use efficiency

than deciduous and graminoid wetland plants (Aerts

et al. 1999). For this reason, it is important to compare NUE, RE, and the resorption proficiency of

similar growth forms and species collected from

nutrient-enriched and unenriched wetlands to assess the vegetation response to eutrophication.

Structural Indicators

Structural indicators of nutrient enrichment consist of community-level attributes like the presence or absence of specific species. Cattail

(Typha), for example, encroaches on and colonizes areas that have undergone soil disturbance,

nutrient enrichment, and hydrology alteration

(Apfelbaum 1985, Urban et al. 1993). Other species are common in nutrient-poor wetlands, but

decline or disappear during eutrophication as they

are overcome displaced (Davis 1989, Craft et

al. 1995, Jensen et al. 1995). Attributes that describe vegetation structure, like biomass and

stem height, also are useful indicators of

enrichment.

Structural indicators of nutrient enrichment include biomass, stem height (discussed earlier),

dramatic/widespread change in plant community

composition over time, and the presence or absence of species adapted to either nutrient-enriched (nutrient-tolerant) or unenriched (nutrient-intolerant) conditions. Biomass and stem

height also provide an index of NPP, which increases in response to enrichment. Other possible structural indicators include species dominance, richness, and the presence of rare and invasive (nonnative) species.

Structural indicators may be less reliable than functional indicators for wetland eutrophication assessments because plants respond to environmental factors other than nutrients. Light, moisture/waterlogging, acidity, and other stressors (e.g., salinity, sulfides, fire) affect plant community composition

(Smith 1996). In addition, different plant species

possess variable life history traits, such as seed production, dispersal, viability, and germination, that

determine their distribution across the landscape (van

der Valk and Davis 1978). Environmental factors

and life history traits interact to regulate the geographic distribution of plant species. Structural indicators, described above, also can be used to assess the overall biological integrity of wetlands.

Module 10: Using Vegetation to Assess Environmental Conditions in Wetlands provides a detailed

overview of using vegetation to assess biological

integrity (Fenessy in press).

Anthropogenic disturbances to wetlands often

are manifested in a dramatic and widespread

change in plant species composition over time.

Aerial and satellite photography can be used to

detect coarse changes in wetland plant communities in response to eutrophication (Jensen et

al. 1987, 1995). Remote sensing techniques can

detect changes in the aerial extent of wetlands,

the percent cover of vegetation, as well as the

replacement of one plant community by another.

Remote sensing requires field verification, however, to calibrate plant community types with

patterns discerned from aerial and satellite images. (See Module 17: Land-Use Characterization for Nutrient and Sediment Risk Assessment,

for further information on this topic.) Field-based

measurements of NPP and biogeochemical indicators also are needed to verify whether eutrophication and not some other type of disturbance (e.g.,

hydrologic alteration) is the causative agent.

During the eutrophication process, large-scale

shifts in plant species composition occur in response

to the addition of the limiting nutrient. For example,

cattail encroaches on and eventually can become

the dominant species in areas of the Everglades that
6

receive large loadings of P, the primary limiting nutrient (Davis 1991). In wetlands where surface

water is present, duckweed (Lemna sp.) often increases in density and coverage in response to increased nutrients (Portielje and Roijackers 1995,

Janse 1998, Vaithiyanathan and Richardson 1999).

Another species that may invade in response to increased nutrients is Phragmites (Chambers et al.

1999, Galatowitsch et al. 1999). It is important to

be aware that some species invade in response to

other anthropogenic alterations like changes in

hydroperiod (e.g., Typha sp., Phragmites australis, Phalaris arundinacea) and salinity (e.g.,

Phragmites, Typha angustifolia) and soil disturbance (Typha sp., Lythrum salicaria,

Phragmites, Phalaris) (Apfelbaum 1985, Urban

et al. 1993, Chambers et al. 1999, Galatowitsch

et al. 1999). Thus, when using species-specific

indicators, it is important to identify anthropogenic disturbances in and around the wetland to

ensure that changes in plant species composition

are the result of nutrient enrichment and not some

other type of disturbance.

In contrast to nutrient-tolerant species, some

species are adapted to low nutrient or oligotrophic conditions. In the Everglades, emergent (sawgrass, Cladium jamaicense) and floating aquatic (bladderwort, Utricularia sp.) vegetation dominate unenriched areas but are replaced by cattail and other species in eutrophic

areas (Davis 1989, Urban et al. 1993). The disappearance of submerged aquatic vegetation

(SAV) also may be a useful indicator of nutrient

enrichment. Over the past few decades, SAV

declined dramatically in many estuaries of the

eastern United States. (Orth and Moore 1983).

The decline of SAV has been linked to light

attenuation caused by eutrophication and sedimentation (Dennison et al. 1993). It should be noted

that species identified as nutrient intolerant may be

limited to specific wetland types and geographic

regions.

A national database of wetland plant sensitivities

to nutrient enrichment and hydrologic alteration is

being produced for USEPA by Paul Adamus of

Oregon State University (Adamus and Gonyaw

2000). The database, which is to include both experimental and observational studies, assesses the

responses of various species to eutrophication and

alteration of wetland hydrology. The database may

serve as a guide to identify wetland species that are

indicators of nutrient enrichment.

Methods for

Assessing Nutrient

Enrichment

A

ssessing wetland to detect nutrient enrichment is different from assessing it for biological integrity. The goals of an Index of Biological

Integrity (IBI) are to assess the health of the biotic or living components of the ecosystem, using metrics such as species richness, and to relate biotic health to anthropogenic stressors, such

as land clearing, drainage, and runoff, that affect

the community undergoing study. The purpose

of this module, in contrast, is to identify vegetation-based indicators of a specific stressor—

eutrophication—whose effects are manifested as

altered ecological structure and function, especially energy flow and nutrient cycles. Despite

their differences, however, both the IBI and the

assessment for nutrient enrichment share a similar framework for achieving their respective

goals. For both types of assessments, it is important to follow the procedures outlined in Module 6: Developing Metrics and IBIs. Like IBIs, assessments for nutrient enrichment should (1) define

clear objectives, (2) classify wetlands into regional

classes, (3) carefully select reference sites and

sample sites, and (4) collect information on wetland characteristics (e.g., hydrology, wetland veg-
7

etation, soils) and surrounding land use. In particular, landscape level and local disturbances that contribute to nutrient enrichment should be identified.

Wetland assessment for eutrophication requires

collection of remotely sensed and field data. Aerial

and satellite photography are used to document

changes in aerial coverage and percent cover of

wetland vegetation as well as coarse changes in plant

community composition over time. Remotely

sensed data are obtained from a variety of government agencies, including NASA; USDA-NRCS;

State highway departments; and local tax, planning,

and zoning offices. Information for obtaining these

data are found in Module 17: Land-Use Characterization for Nutrient and Sediment Risk Assessment.

Field data consist of Level I and Level II indicators of nutrient enrichment that are based on attributes of wetland ecosystem function and structure.

n Level I indicators (stem height, plant tissue N

and P) are relatively easy to measure.

n Level II indicators (aboveground biomass, nutrient use efficiency, presence/absence of nutrient-tolerant and intolerant species) require

greater effort, but better characterize the response of specific structural and functional attributes to nutrient enrichment.

Field Sampling

In addition to remotely sensed data, field and

laboratory measurements are needed to assess

changes in wetland structure and function that occur in response to nutrient enrichment. The best

way to document change in structure and function

is by monitoring the site over time, before and during the eutrophication process. This opportunity

rarely occurs because, in most cases, wetland

eutrophication began decades ago following widespread application of inorganic fertilizers.

A widely used approach to assess anthropogenic

impacts is to compare the ecological integrity of

potentially enriched wetlands with unenriched “reference” wetlands. For example, unenriched areas

of the southern Everglades have been used as a

reference in documenting the effects of enrichment

in areas of the northern Everglades that receive agricultural drainage (Davis 1989, 1991, Craft and

Richardson 1993, 1998, Reddy et al. 1993, Qualls

and Richardson 1995). The ideal reference wetland is one that is relatively undisturbed and possesses the same abiotic template, except for nutrients, as the enriched wetland. When using reference wetlands, a key assumption is that the reference site contains the same assemblage of biota that

enriched wetland contained prior to eutrophication.

Usually, reference wetlands are selected from the

same watershed or from a watershed nearby so

that both enriched and reference wetlands possess

the same abiotic template of climate, geomorphology, geology, hydrology, and soil type.

It is nearly impossible to find wetlands that have

been unaffected by at least some human activity.

Wetlands that are minimally disturbed usually

represent the best approximation. Sampling more

than one reference wetland is highly recommended to fully characterize the natural variability among a particular wetland type and to minimize the effects of human disturbance inherent in

one or more reference sites.

Protocols for field sampling should be designed

to capture the spatial and temporal variability inherent in both candidate and reference wetlands. It

is critical that the same experimental design, frequency of sampling, field measurements, and laboratory methods be used for both nutrient-enriched

and reference wetlands. Because hydrology exerts
8

a controlling influence on wetland structure and function, a stratified sampling approach is needed to

encompass the spatial variation in inundation patterns. Sampling is stratified into deep-, mid-, and

shallow-water zones or from more to less frequently

flooded areas (Figures 1 and 2) (see also Module

6: Developing Metrics and IBIs). Using hydrology

to stratify sampling captures the distinct patterns of

zonation of plant and animal communities that often

are observed in wetlands. Deep-water zones, which

are in contact with water (and nutrients) longer than

shallow-water zones, may respond to enrichment

relatively quickly compared with higher elevations

that are flooded less frequently.

In some wetlands, the presence of inundation

or soil saturation occurs only for short periods

during the growing season. When sampling these

wetlands, it may be necessary to design a sampling plan that encompasses the temporal variability in inundation that affects seasonal changes

in plant and animal communities.

Selection of sampling locations depends on the

size and habitat complexity of the wetland. For

small-sized wetlands or surveys of many wetlands, sampling is stratified according to habitat

complexity or water-level depth. In depressional

or shoreline wetlands, samples and measurements

are taken near the center (deepwater), middle,

and edge (shallow) of the wetland (see Figure

2). In floodplain wetlands, sampling is stratified based on habitat complexity with samples

collected from the levee, oxbow, and terrace

habitats (see Figure 1). Large wetlands or comprehensive studies require greater sampling effort. Comprehensive assessments require replicate sampling points within a given location or

habitat and repeated measurements at a given

location to accurately assess changes in nutrient

indicators over time.

Collection of vegetation for nutrient and carbon

analysis requires careful selection of leaf samples.

When comparing nutrient-enriched and reference

wetlands, it is important that the same species be

sampled in each wetland because different species

possess different amounts of N and P in their leaves

(Craft et al. 1995, Shaver et al. 1998, Aerts et al.

1999). Herbaceous species preferably are sampled

(unless it is a forested wetland) because they grow

faster and respond to enrichment faster than woody

species. The two or three dominant species based

on percent cover or biomass are sampled. It also

is important to collect similar-aged green leaves from

each site, as young leaves usually have higher N

and P content than older leaves (Schlesinger 1991).

In the case of herbaceous vegetation, similar-aged

leaves are selected by clipping leaves from nodes

of a similar distance below the terminal bud. From

woody vegetation, green leaves are selected similarly by sampling a fixed number of nodes (or

branches) below the terminal bud. Replicate leaf

samples are collected from several individual plants

to encompass the variability in leaf N and P within

populations.

A “flow” diagram describing steps for field

sampling of wetland vegetation is provided in

Figure 3.

Analytical Methods

Different methods are required to measure NPP

in herbaceous as opposed to woody vegetation.

For herbaceous vegetation, stem height and biomass are used to measure NPP. Biomass is determined by end-of-season harvest of aboveground

plant material in small (0.25 m2) plots (Broome et

al. 1986). The stem height of individuals of dominant species is measured in each plot. The height

of the 5 to 10 tallest stems in each plot has been

shown to be a reliable indicator of NPP (Broome
9

Upland

loblloly pine 

(Pinus taeda)

white oak 

(Quercus alba)

First Terrace

American elm (Ulmus americana)

sweetgum (Liquidambar styraciflua)

sycamore (Platanus occidentalis)

Second Terrace

willow oak (Quercus phellos)

ironwood (Carpinus caroliniana )

sweetgum(Liquidambar

styraciflua)

River Channel

river birch (Betula nigra)

cottonwood (Populus deltoides)

bald cypress (Taxodium distichum)

Oxbow

bald cypress 

(Taxodium 

distichum)

tupelo gum 

(Nyssa aquatica)

0

20

40

60

80

100

% Time Flooded

Upland

loblloly pine 

(Pinus taeda)

white oak 

(Quercus alba)

First Terrace

American elm (Ulmus americana)

sweetgum (Liquidambar styraciflua)

sycamore (Platanus occidentalis)

Second Terrace

willow oak (Quercus phellos)

ironwood (Carpinus caroliniana )

sweetgum(Liquidambar

styraciflua)

River Channel

river birch (Betula nigra)

cottonwood (Populus deltoides)

bald cypress (Taxodium distichum)

Oxbow

bald cypress 

(Taxodium 

distichum)

tupelo gum 

(Nyssa aquatica)

0

20

40

60

80

100

% Time Flooded

Rarely Flooded

grasses

Occasionally Flooded

Emergents

sedges (Carex)

arrowhead (Saggitaria 

spp.)

Frequently Flooded

Emergents

cattail (Typha spp.)

Continuously Flooded

Floating Aquatics

water lily (Nymphaea spp.)

bladderwort (Utricularia

spp.)

0

20

40

60

80

100

% Time Flooded

Rarely Flooded

grasses

Occasionally Flooded

Emergents

sedges (Carex)

arrowhead (Saggitaria 

spp.)

Frequently Flooded

Emergents

cattail (Typha spp.)

Continuously Flooded

Floating Aquatics

water lily (Nymphaea spp.)

bladderwort (Utricularia

spp.)

0

20

40

60

80

100

% Time Flooded

Figure 1: Distribution of plant species and hydroperiod across

a southeastern bottomland forested wetland.

Figure 2: Distribution of plant species and hydroperiod

across a freshwater marsh wetland.
10

Figure 3: Protocol for sampling vegetation for wetland

eutrophication assessments.

Identify “Impacted” and

Reference Wetlands

Within Each Wetland, Stratify 

Sampling by Plant Community 

or Vegetation Zone. Try to 

Identify Vegetation Zones 

Common to Each Wetland

Within Each Zone, Sample Species/Life 

Forms That are Common to Both 

“Targeted” and Reference Wetlands

For Nutrient Analysis, Clip Similar Age 

Leaves From Several Species in Each 

Zone. Collect Leaves from 5-10 

Individuals of Each Species.
11

et al. 1986) and one that saves the time it takes to

measure the height of all stems in a plot.

Aboveground biomass is clipped at the end of the

growing season, in late summer or fall. If vegetation is dense, 0.25 m2

 plots are sufficient for clipping. Clipped material is separated into live (biomass) versus dead material then dried at 70oC to a

constant weight. For stem height and biomass sampling, 5 to 10 plots per vegetation zone are collected.

For woody vegetation, litterfall is the best technique for measuring NPP. Litterfall is measured by

collecting leaf litter that falls into 0.25 m2 screen or

mesh traps placed on the wetland surface (Chapman

1986). Collections are made periodically (every

1-2 mos.) throughout the year, although collection

during peak litterfall season (Sept.-Dec.) may be

adequate for some assessments.

Leaves are collected and analyzed for N, P,

and organic C. Leaf analyses are performed on

samples that are dried at 70oC. Nitrogen and

organic C are measured by dry combustion using a CHN analyzer. Phosphorus is measured by

spectrophotometry in acid (H2SO4-H2O2) digests

(Allen et al. 1986). Many land-grant universities, state agricultural testing laboratories, and

environmental consulting laboratories perform

these analyses. Contact your local USDA office

or land-grant agricultural extension office for information on laboratories that perform plant tissue nutrient analyses.

Nutrient resorption efficiency, resorption proficiency, nutrient use efficiency, and C:N:P are

calculated from the C, N, and P concentrations

measured previously. Resorption proficiency

and RE require that N and P are analyzed for

both senesced and green tissue (Killingbeck

1996, Aerts et al. 1999). Nutrient use efficiency

requires measurements of productivity (litterfall,

aboveground biomass) and leaf N and P (Vitousek

1982).

For emergent vegetation, community-level indicators (nutrient-tolerant and intolerant species) are

measured in larger plots (2-10 m2), or by estimating percent cover of each species using plot or plotless sampling techniques (Mueller-Dombois and

Ellenberg 1974). The use of community-level indicators with woody vegetation requires larger plots

(0.1–1 ha) or longer transects (Mueller-Dombois

and Ellenberg 1974).

Minimum Monitoring Requirements

Minimum monitoring requirements to assess

nutrient enrichment of wetlands consist of (1) aerial/

satellite photography of the wetland and (2) fieldbased measurements of Level I indicators of enrichment. Level I indicators describe attributes of

wetland structure (stem height) and function (stem

height, leaf C, N, P and C:N:P ratios) that are relatively easy to measure (Table 1).

Remotely sensed data are used to assess coarse

changes in wetland communities over time. Field

measurements such as stem height and leaf N and

P are useful because they respond to nutrient enrichment relatively quickly (Craft et al. 1995,

Chiang et al. 2000). Herbaceous vegetation is a

better indicator of nutrient enrichment than woody

vegetation because herbaceous plants complete

their life cycle in less time and, thus, respond

more quickly to enrichment.

Case Studies

C

ase studies using the Florida Everglades,

Atlantic coast estuarine salt marshes, and

Alaskan wet sedge tundra are presented below to

describe the response of vegetation-based indicators to nutrient enrichment. The response of Everglades plant communities to N and P additions is an

example of phosphorus limitation and eutrophication. The response of the estuarine salt marshes,
12

Measurement Ease of Use Method

Level I

 Functional Indicators

 Stem height (E) 1, 2 Easy Clip plots

 Leaf C and N, C:N Moderate CHN analyzer

 Leaf P, C:P, N:P Moderate Acid digestion & spectrophotometer

 Structural Indicators

 Coarse change in wetland plant communities 

 over time Easy Aerial & satellite photography

Level II

 Functional Indicators

 Aboveground biomass (E) Moderate Clip plots

 Standing dead biomass (E) Moderate Clip plots

 Litterfall (W)1 Difficult Litter traps

 Senesced leaf C, N, C:N 3 Moderate CHN analyzer

 Senesced leaf P, C:P, N:P 3 Moderate Acid digestion & spectrophotometer

 N & P resorption efficiency — Calculated

 Nutrient use efficiency — Calculated

 Structural Indicators

 # of nutrient tolerant species 4 Moderate Plot sampling

 % of nutrient tolerant species 4 Moderate Plot sampling

 # of nutrient intolerant species 4 Moderate Plot sampling

 % of nutrient intolerant species 4 Moderate Plot sampling

1

 E = emergent vegetation, W = woody vegetation.

2

 Structural indicator also.

3

 Resorption proficiency.

4

 Reliable nutrient-tolerant and -intolerant species for most wetlands and geographic regions have not been identified yet.

Note: Level I indicators represent the minimum requirements for assessing enrichment.

Table 1: Level I and Level II indicators of nutrient

enrichment in wetlands
13

which are N-limited, is an example of wetland response to N enrichment. The response of wet sedge

tundra to nutrient enrichment is an example of colimitation by N and P. In the tundra wetland, vegetation-based indicators of nutrient enrichment show

a response to both N and P additions.

Everglades

During the past 10 years, the Florida Everglades

has been the “poster child” for wetland eutrophication. Numerous studies documenting the effects of

N- and P-enriched agricultural drainage on Everglades community structure and ecosystem processes have been published (Davis 1989, 1991,

Craft and Richardson 1993a, 1998, Craft et al.

1995, Reddy et al. 1993, Urban et al. 1993). Ecological changes attributed to nutrient enrichment include increased NPP, tissue P uptake, decomposition, peat accretion, and nutrient accumulation as

well as cattail encroachment into sawgrass and

slough communities (Craft and Richardson 1998,

Qualls and Richardson 2000). Functional indicators of enrichment including aboveground biomass,

stem height, leaf N (standing dead only), and leaf P

were higher in eutrophic areas compared with

unenriched areas (Table 2). Stem density did not

differ between eutrophic (40/m2) and unenriched

sites (38/m2) (Miao and Sklar 1999).

Community-level indicators also responded to increased nutrient loadings. Nutrient- tolerant species including cattail, duckweed (Lemna), and other

species were abundant in eutrophic areas but infrequent in unenriched areas (Table 2), (Craft and

Richardson 1997, Vaithiyanathan and Richardson

1999). Nutrient-intolerant species (e.g., Utricularia spp. and other species) were abundant in

unenriched areas but absent from eutrophic areas

(Table 2) (Vaithiyanathan and Richardson 1999).

The findings presented above were based on

observational data collected from areas of the northern Everglades that receive enormous amounts of

water and nutrients, both N and P. From among

these data, it was difficult to separate the effects of

nutrients from the hydroperiod, and to determine

which responses were due to N versus P. Thus the

causative agent of the observed differences was not

pinpointed.

In 1990, a field experiment was initiated to investigate the effects of N versus P on native Everglades plant communities (Craft et al. 1995,

Chiang et al. 2000). The experiment applied

controlled amounts of N, P, and N+P to plots in

an area of the Everglades unaffected by agricultural water and nutrient loadings. During the first

year of nutrient additions, it became apparent that

P, not N, was the limiting nutrient and, thus, was

responsible for the changes in wetland structure

and function observed in eutrophic areas. After

2 years of P additions, many functional indicators responded to increased P, including increased aboveground biomass, standing dead

material, stem height, and leaf P (Table 3). Leaf

C:P, N:P, resorption efficiency, and NUE (P)

decreased in response to P additions (Table 3).

Sentinel species that reflected low nutrient regimes also responded to P. Utricularia, a floating aquatic plant, declined in response to P and

eventually was replaced by the macroalgae, Chara.

During the 4-year period, no change in species richness or cattail/duckweed encroachment was observed, although other emergents like leather fern

(Acrostichum danaeifolium) increased in response

to P (Table 3). More leaf P and less Utricularia

indicated incipient P enrichment during the first year

of P additions. The response of aboveground biomass to P was not statistically detectable until the

end of the second growing season. Under

unenriched conditions, sawgrass was highly proficient at resorbing P based on standing dead P (70

μg/g) concentrations that were less than 500 μg/g P

as suggested by Killingbeck (1996). There was no

response of vegetation to N additions (data not

shown), indicating that P, not N, limits productivity

and leads to eutrophication in this wetland system.
14

Indicator Unenriched Eutrophic

Functional Indicators

 Stem height (cm)1 160 205

 Aboveground biomass (g/m2)

1 976 1958

 Stem density (number/m2)

1 38 40

 Leaf N (%)1 0.70 0.70

 Leaf P (μg/g)1 250 650

 Leaf N:P (wt:wt)1 28 11

 Standing dead N (%)2 0.40 0.56

 Standing dead P (μg/g)2 80 375

 Standing dead N:P (wt:wt)2 38 15

Structural Indicators

 Course change in wetland plant

 communities over time3 No change Decreased sawgrass, increased cattail

 Nutrient-intolerant species

 Utricularia spp.4 Abundant Absent

 Nutrient-tolerant species

 Typha4,5 Infrequent Abundant

 Lemna4 Absent Abundant

 Acrostichum danaeifolium4

Infrequent Common

1

 From Miao and Sklar (1999)

2

 From Davis (1991)

3

 Jensen et al. (1995)

4

 From Vaithiyanathan and Richardson (1999)

5

 From Craft and Richardson (1997)

Note: Numerical values in bold reflect statistically significant differences (p>0.05) between unenriched and

eutrophic conditions.

Table 2: Comparison of vegetation-based indicators of phosphorus (P)

enrichment in unenriched and eutrophic sawgrass, Cladium jamaicense,

communities of the Florida Everglades
15

Indicator Response Response Time

Unfertilized

(no P)

Fertilized

(4.8 g P/m2/yr)

Level I

 Stem height1 — — 1-2 years

 Leaf P (μg/g) 210 530 <1year

 Leaf C:P (wt:wt) 2100 840 <1 year

 Leaf N:P (wt:wt)2 29 12 <1 year

Level II

 Aboveground biomass (g/m2) 1160 2950 1-2 years

 Standing dead biomass (g/m2) 1520 3670 —3

 Standing dead P (μg/g) 74 398 —3

 Standing dead C:P (wt:wt) 6000 1100 —3

 Standing dead N:P (wt:wt)4 51 11 —3

 Resorption efficiency (P) 54% 7% —3

 Resorption proficiency (P, %)5

.007 .04 —3

 NUE(P) 13500 2500 1-2 years

 Nutrient-intolerant species (g/m2)

 (Utricularia)6 200 30-50 <1 year

 Nutrient-tolerant species (g/m2)

 (Chara)6 0 70-180 1-2 years

 (Acrostichum danaeifolium)7 0 400 1-2 years

 (Typha)7 45 60 No change

 (Lemna)1 — — No change

Table 3: Level I and Level II indicators of phosphorus (P) enrichment

of sawgrass, Cladium jamaicense, communities in the

Florida Everglades

1

 Determined by visual inspection.

2

 Leaf N content of unfertilized and fertilized plots was 0.60% andn 0.65%, respectively.

3

 Measured during year 3 of the study.

4

 Standing dead N content of unfertilized and fertilized plots was 0.38% and 0.45%, respectively.

5

 Same as standing dead P.

6

 Slough community.

7

 Mixed sawgrass-cattail community.

Notes: The response to P was measured over a 4-year period. In this study, there was no response to P additions. Numerical values

in bold indicate that phosphorus-fertilized and unfertilized plots were statistically different (p<0.05) from each other.

Source: Data are from Craft et al. 1995, Chiang et al. 2000.
16

Results from the Everglades experiment indicate

that (1) reliable vegetation-based indicators of P

enrichment exist and (2) some indicators (e.g., leaf

P, Utricularia) respond more rapidly to increased

P than others. The rapid and consistent responses

of leaf P, NPP, and Utricularia suggest that these

indicators are reliable for monitoring conditions in

the Everglades. Other indicators, like cattail and

duckweed encroachment, were not observed during the first 4 years of the experiment. The absence

of cattail encroachment into the fertilized plots probably reflects the fact that competitive displacement

is a time-dependent process (Mal et al. 1997). A

shift in emergent species composition in the fertilized plots might take longer than the 4-year period

of record of the experiment. Furthermore, the reported increase of cattail and duckweed in eutrophic

areas of the Everglades may be the result of increased water depth in addition to P enrichment

(Urban et al. 1993).

Estuarine Salt Marshes

Like Everglades vegetation, salt marsh vegetation responded quickly when the primary limiting nutrient, in this case N, was added. Leaf N

and aboveground biomass of Spartina

alterniflora, the dominant species in east coast

salt marshes, increased during the first year of N

additions (Table 4). Leaf C:N, standing dead N,

and NUE(N) also increased relative to unfertilized plots during the first year of N fertilization

(Table 4). Stem height, a Level I indicator, also

increased in response to N additions, although

the response was not significantly different from

unfertilized plots. Because nitrogen is a component of chlorophyll, where photosynthesis takes

place, N additions quickly translate into increased

aboveground biomass. Many studies report that

leaf N and aboveground biomass increase within a

few months after N is added (Valiela and Teal 1974,

Broome et al. 1975, Chalmers 1979). Additions

of N sometimes produce more flowering stems of

Spartina whereas P additions increase the number

of flowering stems even more (Broome et al. 1975).

Wet Sedge Tundra

Nutrient additions to wet sedge tundra communities in Alaska revealed that tundra vegetation

responded to additions of either N, P, or N+P

(Shaver et al. 1998) (Table 5). After 5 years of

fertilization, leaf N and aboveground biomass

increased in response to N additions, whereas

C:N and N:P decreased in N-treated plots. The

effect of P additions on functional indicators of

enrichment was even more pronounced than with

N. Leaf P and aboveground biomass increased

dramatically in response to P additions whereas

leaf C:P and N:P decreased in P-treated plots

(Table 5). The plant response to N+P additions

was greater as compared with either N or P applied singly, indicating that tundra communities

are limited primarily by P and secondarily by N

(Shaver et al. 1998). In a separate fertilization experiment, Shaver and Chapin (1995) added N, P,

and K to moist tussock and wet sedge vegetation

in the Alaskan tundra. Similar to the Everglades

case study, leaf N and P increased following the

first year of nutrient additions. Increased plant

growth and biomass production was not observed

until year 2 of the study and, in year 3, flowering

increased in response to fertilizer additions.

In salt marshes and amid tundra vegetation, leaf

N concentrations declined after the first year of

N fertilization, as N was “diluted” by enhanced

biomass production (Valiela and Teal 1974,

Shaver and Chapin 1995). However, loss of sensitivity of this Level I indicator was offset by

increased NPP, aboveground biomass, and stem

height. In contrast to N, in ecosystems where P

was limiting or co-limiting, leaf P concentrations

remained elevated even as NPP increased in response to P enrichment (Shaver and Chapin 1995,

Chiang et al. 2000).
17

The results of the Everglades, salt marsh, and tundra fertilization studies demonstrate that increased

leaf nutrient (N, P) content is a powerful indicator

of eutrophication because it is among the first to

respond to nutrient enrichment. Level I (stem height)

Indicator Response Response Time

Unfertilized +N

Level I

 Stem height (cm)1 77 103 <1 year

 Leaf N (%)1 0.82 1.05 <1 year

 Leaf C:N (wt:wt)1,2 49 38 <1 year

Level II

 Aboveground biomass (g/m2)

1 360 600 <1 year

 Standing dead N (%)3,4 0.90 1.05 <1 year

 NUE(N) 111 95 <1 year

1

 From Broome et al (1975), N added as ammonium sulfate at a rate of 16.2 g N/m 2/yr.

2

 Leaf C is assumed to be 40%.

3

 From Chalmers (1979), N added as sewage sludge at a rate of 2 g N/m 2/wk.

4

 Same as Resorption Proficiency.

Notes: In this study (Broome et al. 1975), N was the primary limiting nutrient and P (data not shown) was

secondarily limiting. Numerical values in bold indicate that phosphorus-fertilized and -unfertilized plots were

statistically different (p<0.05) from each other.

Table 4: Level I and Level II indicators of nitrogen (N) enrichment

of Spartina alterniflora dominated salt marshes along the

Atlantic (NC, GA) coast

and II (aboveground biomass) metrics of NPP likewise respond relatively quickly to nutrient enrichment. They, too, are useful detectors of incipient

eutrophication of wetlands.
18

Indicator Response Response

Time1

Unfertilized

(no N or P) +N (10 g/m2

/yr) +P (5 g/m2/yr) N+P

Level I

Leaf N (%) 1.48 a 1.78 b 1.46 a 1.69 b <1 yr

Leaf P (ug/g) 830 a 1120 b 2660 b 3870 b <1 yr

 Leaf C:N (wt:wt)2 27.0 22.5 27.4 23.7 <1 yr

 Leaf C:P (wt:wt)2 482 357 150 103 <1 yr

 Leaf N:P (wt:wt)2,3 17.8 15.9 5.5 4.4 <1 yr

Level II

 Aboveground biomass (g/m2) 142 a 195 b 283 c 404 d 1-2 yr

1

 Response time was based on an earlier study by Shaver and Chapin (1995).

2

 No statistical analyses were performed on these parameters.

3

 Leaf C was assumed to be 40%.

Notes: In this study, indicators of nutrient enrichment responded to additions of either N, P, or N+P, indicating that both N

and P limit plant productivity of this community. Numerical values within the same row separated by the same letter were not

statistically different (p<0.05) from each other.

Source: Data are from Shaver et al. 1998.

Table 5: Level I and Level II indicators of nitrogen (N) and

phosphorus (P) enrichment of a wet sedge tundra (Eriophorum

angustifolium) in Alaska after 5 years of fertilization
19

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Glossary

Nutrient resorption proficiency The absolute

or lowest levels to which nutrient concentrations are

reduced in senesced (dead) leaves.

Nutrient use efficiency (NUE) Aboveground

biomass production (e.g., g litterfall/m2) divided

by quantity of nutrient (e.g., g N/m2) in litterfall.

Structural indicators Attributes that describe

community-level characteristics of ecosystems

like species richness, species diversity, and

canopy architecture (e.g., stem height, vertical

stratification).

Ecological integrity The capacity of an ecosystem to sustain essential life support services such as

energy flow, biogeochemical cycling, niche space,

and habitat.

Functional indicators Attributes that describe

ecosystem function, like energy flow (e.g., productivity) and biogeochemical (e.g., nitrogen,

phosphorus) cycling.

Nutrient resorption efficiency (r) Amount of

nutrients (e.g., N or P) resorbed from mature

leaves divided by maximum nutrient pool in mature leaves (expressed as g/m2

).